Soil-borne pathogens are a key component of the belowground community because of the significance of their ecological and socio-economic impacts. For instance, several species of Phytophthora and Pythium, two well-known genera of soil-borne oomycete pathogens, are common causes of agricultural diseases (Erwin & Ribeiro, 1996; Martin & Loper, 1999) and are involved in the massive decline of Quercus, Castanea, Eucalyptus and other trees in forests worldwide (Brasier et al., 1993; Brasier, 1996; Rizzo et al., 2005; Romero et al., 2007; Cahill et al., 2008). Not surprisingly, an understanding of when and where soil-borne pathogens are more likely to cause destructive epidemics has long been an important topic of agricultural research. In natural systems, however, much less is known about the complexity of their distribution patterns, which remains one of the most challenging aspects of studying belowground organisms (Ettema & Wardle, 2002; Reinhart & Clay, 2009).
The pathogen landscape can be affected by a variety of abiotic and biotic factors (Martin & Loper, 1999; Agrios, 2005). Among these factors, vegetation is a major determinant of the spatial distribution of soil pathogens both across and within plant species (Wardle, 2002). Plant species can affect soil-borne pathogen populations directly by providing living host tissue, or indirectly by generating environmental conditions that affect their reproductive activity (Augspurger, 1990). In forest ecosystems, for example, pathogen populations can benefit from the wetter microclimatic conditions found in the shaded understory relative to open environments (Gómez, 2004; Matías et al., 2011). However, understory environments tend to have more fertile soils than gaps and sustain a larger microbial community, which could negatively affect soil-borne pathogens through competition for resources and colonization space (Weste & Marks, 1987; Aponte et al., 2010). Depending on the relative importance of the different mechanisms, the net effect of a given woody species on soil pathogen abundance might range from highly positive to largely negative. However, species-specific effects could be obscured by intraspecific variation in plant traits, such as size or tolerance to infection (Packer & Clay, 2000, 2003; Reinhart & Clay, 2009). Clearly, further research is needed in order to determine whether and how the mosaic of plant species and gaps in the forest canopy translate into a mosaic of soil pathogen abundance and composition.
Just as adult plants can drive the abundance and activity of soil-borne pathogens in forests, pathogens can, in turn, shape the regeneration dynamics of the plant community (Packer & Clay, 2003; O’Hanlon-Manners & Kotanen, 2006). Seedlings are particularly vulnerable to pathogens because their roots are structurally simple and poorly lignified (Augspurger, 1984, 1990; Romero et al., 2007). Moreover, because pathogens vary in pathogenicity for different tree species (Augspurger & Wilkinson, 2007; Moralejo et al., 2009; Reinhart et al., 2010), they can affect the composition of the seedling bank. For example, it has been proposed that shade-intolerant tree species are more susceptible to soil-borne diseases than are shade-tolerant species, and that such susceptibility might be a key mechanism excluding them from the forest understory (O’Hanlon-Manners & Kotanen, 2004; McCarthy-Neumann & Kobe, 2008). If differential responses to soil pathogens exist, interactions with soil-borne pathogens may contribute to species coexistence across heterogeneous forests.
The objective of this article was twofold. First, we aimed to advance the understanding of the pathogen landscape by developing spatially explicit neighborhood models that explain the importance of abiotic (soil texture) and biotic (tree and shrub community) drivers of soil-borne pathogen abundance in Mediterranean forests affected by cork oak (Quercus suber) decline. We built on established methods for the characterization of neighborhood processes (Canham & Uriarte, 2006), and applied these methods for the first time on soil organisms in close association with plants. A main advantage of the neighborhood approach is that it allows the linking of soil pathogen abundance with the distribution of neighboring individuals of the whole woody community. It therefore captures the complexity of natural plant communities, in which a particular volume of soil is not necessarily occupied by just one host species. The second objective of our study was to explore the consequences of soil-borne pathogen abundance on seedling emergence and survival of dominant tree species with varying shade tolerance (Quercus canariensis > Q. suber > Olea europaea var. sylvestris). For this, we conducted an in situ field experiment in which seeds of the three tree species were sown and monitored in the same locations in which pathogen abundance was quantified. To the best of our knowledge, this is the first study that simultaneously analyzes the spatial relationship among abiotic soil properties, adult plants (trees and shrubs), and the pathogen and seedling community in a multispecies natural context.